SUMMARY

An understanding of the evolution of human bipedalism can provide valuable
insights into the biomechanical and physiological characteristics of
locomotion in modern humans. The walking gaits of humans, other bipeds and
most quadrupedal mammals can best be described by using an inverted-pendulum
model, in which there is minimal change in flexion of the limb joints during
stance phase. As a result, it seems logical that the evolution of bipedalism
in humans involved a simple transition from a relatively stiff-legged
quadrupedalism in a terrestrial ancestor to relatively stiff-legged bipedalism
in early humans. However, experimental studies of locomotion in humans and
nonhuman primates have shown that the evolution of bipedalism involved a much
more complex series of transitions, originating with a relatively compliant
form of quadrupedalism. These studies show that relatively compliant walking
gaits allow primates to achieve fast walking speeds using long strides, low
stride frequencies, relatively low peak vertical forces, and relatively high
impact shock attenuation ratios. A relatively compliant, ape-like bipedal
walking style is consistent with the anatomy of early hominids and may have
been an effective gait for a small biped with relatively small and less
stabilized joints, which had not yet completely forsaken arboreal locomotion.
Laboratory-based studies of primates also suggest that human bipedalism arose
not from a terrestrial ancestor but rather from a climbing, arboreal
forerunner. Experimental data, in conjunction with anatomical data on early
human ancestors, show clearly that a relatively stiff modern human gait and
associated physiological and anatomical adaptations are not primitive
retentions from a primate ancestor, but are instead recently acquired
characters of our genus.

Introduction

One of the features that separate humans from all other primates is the
habitual use of a bipedal gait. This single feature is seen as such a defining
characteristic that skeletal adaptations to bipedalism are used to identify
our extinct hominid ancestors. Yet, because of the paucity of the fossil
record, the fragmentary nature of fossil remains, and the difficulty of
inferring behavior from fossils, significant questions remain unanswered
concerning the evolution of human bipedalism. Over the past thirty years,
however, experimental analyses of locomotion in humans and other primates have
done much to improve our understanding of the mechanics of human locomotion
and have provided insights into the evolutionary origins of modern human
bipedalism.

When modern humans walk, we vault over relatively stiff lower limbs in such
a way that our center of mass is at its lowest point at heel-strike and rises
to its highest point at midstance (Cavagna
et al., 1976; Lee and Farley,
1998). This inverted pendulum-like gait allows for an effective
exchange of gravitational potential and kinetic energy
(Cavagna et al., 1976). The
same style of walking is employed by other bipeds and probably by most
quadrupeds (Cavagna et al.,
1976,
1977;
Alexander, 1977;
Heglund et al., 1982;
Gatesy and Biewener, 1991;
Griffin and Kram, 2000; Farley
and Ko, 2000; Griffin, 2002).
Thus, it might seem reasonable to argue that the evolution of human bipedalism
was a logical progression from a relatively stiff quadrupedal walking style to
our modern gait. Evidence from numerous experimental studies, however,
suggests that the evolution of bipedalism was much more complicated.
Understanding the nature of locomotion in our prebipedal primate ancestor
(prehominid) and in early hominid bipeds has the potential to provide unique
insights into the basic mechanics of walking in humans and other animals.

Primate locomotor characteristics

Primates show a remarkable diversity of locomotor behaviors. The apes
(gibbons, orangutans, chimpanzees and gorillas) show a particularly wide range
of locomotor habits, including acrobatic arm-swinging, quadrumanous climbing,
quadrupedal knuckle- or fist-walking, and regular short bouts of bipedal
locomotion. Nonetheless, quadrupedalism is the most common mode of locomotion
among primates, and the ways in which primate quadrupedalism is similar to or
differs from that of other mammals has bearing on the pathways for the
evolution of more specialized forms of locomotion, including bipedalism.

Data from laboratory-based studies of primate locomotion, much of which is
summarized below, can be of great utility to those working on locomotor
mechanics in other vertebrates. To make the reader aware of what data are
available, I have included a representative list of major studies of primate
locomotor mechanics (Table 1).
Below, however, I concentrate only on those studies that bear directly on the
unique aspects of primate locomotion and the evolution of human
bipedalism.

Summary of the commonly accepted differences that are believed to
distinguish the walking gaits of most primates from those of most nonprimate
mammals. Nonprimates generally use (A) lateral sequence walking gaits (LH, RH,
left and right hindlimb; LF, RF, left and right forelimb), (B) have a humerus
that at ground contact is retracted relative to a horizontal axis passing
through the shoulder, and (C) have greater peak vertical forces F on
their forelimbs than they do on their hindlimbs. Primates show the opposite
pattern. From Schmitt and Lemelin
(2002), with permission.

Primate locomotor evolution

The gait characteristics thought to distinguish most primates from most
other mammals have all been associated directly or indirectly with the
mechanical requirements of locomotion on thin flexible branches
(Schmitt and Lemelin, 2002;
Cartmill et al., 2002;
Schmitt, 2003a), an
environment thought to be critical in the origin of primates fifty-five
million years or more ago (Cartmill,
1974; Fleagle,
1999). This combination of gait characteristics, shown by primates
in general and arboreal primates especially, results in a strong functional
differentiation between forelimbs and hindlimbs. This may have facilitated the
use of forelimbs in tension during climbing and arm-swinging in New World
monkeys and apes. This suite of gait characteristics that typify primates may
ultimately have played a role in the evolution of bipedalism (Stern,
1971,
1976;
Reynolds, 1985;
Schmitt, 1998;
Larson et al., 2001;
Schmitt and Lemelin,
2002).

The skeleton of one individual of Australopithecus afarensis.
Members of this early hominid species were relatively small and short, with
females weighing approximately 30 kg and standing about 1.05 m tall (McHenry
1991b,
1992). These early hominids
were gracile with small and loosely stabilized limb and vertebral joints and
distinctly curved phalanges (Stern and
Susman, 1983), features that are also found in many extant apes.
Like living apes, they also had relatively long upper limbs compared to the
lower limbs, a condition that is also found in later australopithecines
(McHenry and Berger, 1998).
Many of the ape-like features of the postcranial skeleton are also found in
earlier australopithecines (Ward et al.,
1999). Exactly how these features should be interpreted is the
subject of considerable debate (Susman et
al., 1984; Latimer,
1991; Stern,
2000; Lovejoy et al.,
2002; Ward,
2002), although the joint morphology suggests a different loading
pattern from that found in modern humans
(Stern and Susman, 1983;
Schmitt et al., 1996,
1999). The image is modified
from Fleagle (1999).

Angular values for the lower limb joints of humans walking normally and
compliantly compared with bipedal walking gaits of the gibbon (Hylobates
lar) and the pygmy chimpanzee (Pan paniscus). The data for the
humans were collected at SUNY Stony Brook using the same sample as was used
for the maximum walking speed and stride length data presented in
Table 2. The data for the
gibbon are a composite of data from Prost
(1967) and Yamazaki and
Ishida (1984). The data for
the chimpanzee are from D'Aout et al.
(2002).

Since nonhuman primates typically utilize compliant gaits when they walk
either quadrupedally or bipedally, it seems plausible then, that early bipedal
hominids would have retained a compliant walking style typical of other
nonhuman primates. Postcranial anatomy of early hominids suggests that some of
them walked with a deeply yielding knee and hip
(Stern and Susman, 1983). But
beyond being simply a primitive retention, compliant walking in prehominids
may have had several advantages. Among quadrupedal nonhuman primates, low peak
forces and reduced stride frequencies make their locomotion relatively smooth,
which helps them avoid shaking flexible branches, thus enhancing their
stability and helping them escape the notice of predators
(Demes et al., 1990; Schmitt,
1998,
1999). These features may
have also allowed primates to maintain mobile, loosely stabilized forelimb
joints. Our recent kinematic, force plate and accelerometer studies on human
compliant bipedalism (summarized in Table
2) show that humans who adopted a complaint gait achieved longer
stride lengths, faster maximum walking speeds, lower peak vertical forces, and
improved impact shock attenuation between shank and sacrum compared to normal
walking (Schmitt et al.,
1996,
1999). These data are
consistent with findings of several other studies
(Yaguramaki et al., 1995;
Li et al., 1996). As a
result, my colleagues and I have argued, as did Stern and Susman
(1983), that compliant
bipedalism may have been an effective gait for a small biped, with relatively
small and weakly stabilized joints that had not yet completely forsaken
arboreal locomotion (Schmitt et al.,
1996,
1999).

The effect of compliant bipedalism on temporal and kinetic variables in
humans

Humans who attempt to walk with a compliant gait often find it awkward,
however, and some researchers argue that the retention of compliant walking
style in early hominids is unlikely because it would be too energetically
expensive and raises core-body temperatures
(Crompton et al., 1998). It is
likely that a modern bipedal walking gait would be more efficient than
hominoid-style quadrupedalism or bipedalism (Leonard and Robertson,
1995,
1997a,b,
2001). Some have argued that
the costs of locomotion would be especially high for a short-legged hominid
(Jungers, 1982;
Rodman and McHenry, 1980; but
for a contrary view, see Kramer,
1999). However, a review of the literature by Stern
(1999) suggests that the
differences would have been minor. Moreover, there is little evidence that
such a compliant bipedal gait in early hominids would have been more
energetically costly than that of a quadrupedal prehominid. Experimental
studies have repeatedly shown that there is little difference in energetic
costs between quadrupeds and bipeds
(Taylor and Rowntree, 1973;
Fedak et al., 1977;
Fedak and Seherman, 1979;
Rodman and McHenry, 1980;
Roberts et al.,
1998a,b;
Griffin, 2002), although a
recent study found a 20% increase in cost in macaques
(Nakatsukasa et al., 2002).
In addition, Steudel (Steudel,
1994,
1996;
Steudel-Numbers, 2001), using
data on limb length and oxygen consumption for humans and other mammals,
concluded that `increased energetic efficiency would not have accrued to early
bipeds' (Steudel, 1996, p.
345). She goes on, however, to point out that `selection for improved
efficiency in the bipedal stance would have occurred once the transition [to
modern human bipedalism] was made'
(Steudel, 1996, p. 345). In
summary, it certainly cannot be convincingly argued that bipedalism in the
earliest hominids provided significant savings in energy. By the same token,
it is unlikely that a shift to bipedalism induced significant energetic costs
relative to the locomotion of a prehominid primate.

Locomotion of the prehominid primate

Although a discussion of the selective advantages of bipedalism is beyond
the scope of this paper, one other way to understand the pathway through which
bipedalism evolved is to consider the mode of locomotion in the prebipedal
prehominid ancestor. The mode of locomotion in the primate that immediately
preceded the adoption of upright bipedalism has been a subject of debate since
the turn of the last century (for thorough reviews, see
Tuttle, 1974;
Richmond et al., 2002).
Theories concerning the nature of locomotion in the prehominid primate can be
divided into three basic groups. The troglodytian model posits a terrestrial,
knuckle-walking chimpanzee as the prototype for a prehominid (e.g.
Washburn, 1951; Gebo,
1992,
1996;
Richmond et al., 2002).
Proponents of this model argue for a significant component of terrestrial
locomotion in the hominid ancestor (Gebo,
1992) but do not preclude arboreal activity as a significant
component of the evolution of bipedalism
(Richmond et al., 2002). In
addition, some researchers have argued that feeding, not locomotor,
adaptations in chimpanzees are critical for the evolution of hominid
bipedalism (Hunt, 1994;
Stanford, 2002). Supporters
of a brachiationist model alternatively suggest that bipedalism evolved from a
small-bodied suspensory ancestor similar to gibbons (e.g.
Keith, 1923;
Tuttle, 1981). Finally, other
researchers invoke no specific primate as a distinct model for the prehominid,
but argue instead that the mechanical requirements of climbing vertical
supports are similar to those required by early bipeds
(Stern, 1971;
Prost, 1980;
Fleagle et al., 1981). Of
course, these models are not mutually exclusive, and some have argued for an
ancestor with a varied and generalized locomotor repertoire
(Rose, 1991). These models
can be evaluated using phylogenetic, morphometric, fossil and experimental
evidence, but these approaches do not yield consistent results.

While phylogenetic evidence points toward chimpanzees, and fossil evidence
remains ambiguous, experimental studies of humans and other primates point
squarely toward an arboreal, climbing ancestor of hominids, because the
mechanics of arboreal climbing and bipedalism are more similar to each other
than either is to the mechanics of terrestrial quadrupedalism. Some of the
earliest experimental work on locomotion in apes was carried out independently
by Russell Tuttle of the University of Chicago and Jack Stern of the State
University of New York at Stony Brook. Tuttle's studies of muscle recruitment
patterns in forearm and gluteal musculature in chimps and gorillas led him and
his colleague John Basmajian to conclude that terrestrial quadrupedalism did
not play a critical role in the evolution of bipedalism. Rather they surmised
that `hominid bipedalism may indeed be rooted in bipedal reaching and
branch-running behaviors of relatively small bipedal apes'
(Tuttle and Basmajian, 1974a,
p. 312).

Stern and his colleagues documented recruitment patterns of forelimb and
hindlimb muscles in a variety of ape and monkey species
(Stern et al., 1977;
Vangor, 1977;
Fleagle et al., 1981;
Stern and Susman, 1981;
Vangor and Wells, 1983).
Perhaps the most critical result of their studies was the finding that spider
monkeys, chimpanzees and orangutans recruit their lesser gluteal muscles to
the greatest degree during stance phase of vertical climbing and bipedalism to
produce medial rotation of the femur or to stabilize the pelvis when walking
with a flexed hip (Fig. 5).
They concluded that a transition from vertical climbing to bipedalism would
have involved minimal change in the functional role of thigh musculature.
These data, along with additional EMG and bone strain data, led them to
conclude that a prehominid primarily adapted for vertical climbing would
develop `hindlimb morphology pre-adaptive for human bipedalism'
(Fleagle et al., 1981, p.
360). Ishida et al. (1985)
reached the same conclusion in their electromyographic study of bipedal
walking in a variety of primate species. The argument that vertical climbing
is a `good intermediate between arboreal behavior and terrestrial bipedalism'
(Prost, 1985, p. 301) is
further supported by kinematic and electromyographic data on gibbons,
chimpanzees and spider monkeys walking bipedally and climbing vertical
supports (Prost, 1967,
1980; Hirasaki et al.,
1993,
1995,
2000).

Electromyographic activity of gluteus medius in spider monkeys
(Ateles sp.) and chimpanzees (Pan troglodytes) during
terrestrial quadrupedalism, terrestrial bipedalism, and climbing a large
vertical support. The data for the spider monkey are from Fleagle et al.
(1981), and for the chimpanzee
from Stern and Susman (1983).
The graphs follow the approach of Stern et al.
(1980). The x-axis
represents stance and swing phase. The y-axis represents activity
(expressed as a percentage of maximum muscle recruitment) that occurred 75% of
the time during the respective activity. Muscular recruitment increases in
both magnitude and duration from quadrupedalism to bipedalism. The recruitment
patterns during bipedalism and vertical climbing are similar to each other.
The same pattern is found for the orangutan (Pongo pygmaeus) for all
three behaviors and for the gibbon (Hylobates lar) during bipedalism
and vertical climbing (Stern and Susman,
1983).

Additional support for an arboreal/climbing ancestry for hominids comes
from force-plate studies showing that the difference in forelimb and hindlimb
peak vertical forces is greatest in highly arboreal primates
(Kimura et al., 1979; Kimura,
1985,
1992;
Reynolds, 1985;
Demes et al., 1994;
Schmitt and Lemelin, 2002).
More recent studies show that functional differentiation between fore- and
hindlimbs is greatest when animals walk on arboreal supports or climb vertical
poles (Hirasaki et al., 1993,
2000;
Schmitt, 1998;
Wunderlich and Ford, 2000).
Data on peak plantar pressures in chimpanzees and humans led Wunderlich and
Ford (2000) to state that
chimpanzee quadrupedal walking on arboreal supports resembles human bipedalism
more closely than either chimpanzee terrestrial quadrupedalism or bipedalism.
Thus, if reducing the weight-bearing role of the forelimbs is critical to the
evolution of bipedalism, it seems likely that the hominid ancestor was an
active arborealist. Recent experimental studies associating heel-strike at the
end of swing phase with arboreal quadrupedalism
(Schmitt and Larson, 1995)
and vertical climbing (Wunderlich and
Schmitt, 2000) further strengthen this argument.

Conclusions

Experimental data collected on humans and nonhuman primates suggest that
early hominid bipedalism evolved in an arboreal, climbing primate. The
earliest mode of bipedalism included many aspects of locomotion seen in modern
humans, but probably did not involve inverted pendulum-like mechanics. This
difference in locomotor styles between early hominids and modern humans
appears to be associated with small, gracile and poorly stabilized hindlimbs
in our earliest ancestors (Stern and
Susman, 1983). It seems likely that the shift to a more robust
modern skeleton seen in early members of the genus Homo reflected the
adoption of a relatively stiff-legged gait. This perspective on the evolution
of bipedalism from a relatively compliant to a relatively stiff-legged style
changes our understanding of locomotor adaptations in the genus Homo.
The data described above strongly suggest that a relatively stiff-legged
bipedal gait and associated physiological and musculoskeletal adaptations are
not inherited from prebipedal ancestors or even from the earliest upright
bipeds. These features are instead, specialized characters that evolved
relatively recently.

ACKNOWLEDGEMENTS

I am grateful to Matt Cartmill, Tim Griffin, Laura Gruss, Mark Hamrick,
Jandy Hanna, Susan Larson, Pierre Lemelin, Brian Richmond, Jack Stern,
Christine Wall and Roshna Wunderlich for insightful discussions, comments and
advice in the preparation of this manuscript. I thank Ruth Hein for skilful
editing. The comments of two anonymous reviewers significantly improved this
manuscript. Much of the research on primate and human compliant walking was
supported by the National Science Foundation (SBR 8819621, 89044576, and
9209004; BCS 990441), the L. S. B. Leakey Foundation, and Sigma Xi.

Berge, C. (1984). Multivariate analysis of the
pelvis for hominids and other extant primates: Implications for the locomotion
and systematics of the different species of Australopithecines. J.
Hum. Evol.13,555
-562.

Gruss, L. T. and Schmitt, D. (in press). Bipedalism in
Homo Ergaster: An experimental study of the effects of tibial
proportions on locomotor biomechanics. In From Biped to Strider:
The Emergence of Modern Human Walking, Running and Resource
Transport (ed. J. Meldrum and C. Hilton). New York:
Kluwer/Plenum.

Larson, S. G. and Stern, J. T. (1989). The role
of propulsive muscles of the shoulder during quadrupedalism in vervet monkeys
(Cercopithecus aethiops): implications for neural control of
locomotion in primates. J. Motor Behav.21,457
-472.